Sub- and Supramolecular X-Ray Characterization of Engineered Tissues from Equine Tendon, Bovine Dermis, and Fish Skin Type-I Collagen.


Journal

Macromolecular bioscience
ISSN: 1616-5195
Titre abrégé: Macromol Biosci
Pays: Germany
ID NLM: 101135941

Informations de publication

Date de publication:
05 2020
Historique:
received: 13 01 2020
accepted: 23 01 2020
pubmed: 13 3 2020
medline: 4 6 2021
entrez: 13 3 2020
Statut: ppublish

Résumé

Collagen represents one of the most widely used biomaterial for scaffolds fabrication in tissue engineering as it represents the mechanical support of natural tissues. It also provides physical scaffolding for cells and it influences their attachment, growth, and tissue regeneration. Among all fibrillary collagens, type I is considered one of the gold standard for scaffolds fabrication, thanks to its high biocompatibility, biodegradability, and hemostatic properties. It can be extracted by chemical and enzymatic protocols from several collagen-rich tissues, such as tendon and skin, of different animal species. Both the extraction processes and the manufacturing protocols for scaffolds fabrication provide structural and mechanical changes that can be tuned in order to deeply impact the properties of the final biomaterial. The aim of this review is to discuss the role of X-rays to study structural changes of type I collagen from fresh collagen-rich tissues (bovine, equine, fish) to the final scaffolds, with the aim to screen across available collagen sources and scaffolds fabrication protocols to be used in tissue regeneration.

Identifiants

pubmed: 32163225
doi: 10.1002/mabi.202000017
doi:

Substances chimiques

Collagen Type I 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

e2000017

Informations de copyright

© 2020 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim.

Références

R. P. Mecham, Curr. Protoc. Cell Biol. 2012, 1, 10.1.1.
P. Lu, K. Takai, V. M. Weaver, Z. Werb, Cold Spring Harbor Perspect. Biol. 2011, 3, a005058.
A. Aszódi, K. R. Legate, I. Nakchbandi, R. Fässler, Annu. Rev. Cell Dev. Biol. 2006, 22, 591.
T. Rozario, D. W. DeSimone, Dev. Biol. 2010, 341, 126.
S. V. Plotnikov, A. M. Pasapera, B. Sabass, C. M. Waterman, Cell 2012, 151, 1513.
J. D. Humphrey, E. R. Dufresne, A. M. Schwartz, Nat. Rev. Mol. Cell Biol. 2014, 15, 802.
C. Frantz, K. M. Stewart, V. M. Weaver, J. Cell Sci. 2010, 123, 4195.
B. Alberts, A. Johnson, J. Lewis, M. Raff, K. Roberts, Ann. Bot. 2003, 91, 401.
A. Terzi, E. Storelli, S. Bettini, T. Sibillano, D. Altamura, L. Salvatore, M. Madaghiele, A. Romano, D. Siliqi, M. Ladisa, L. De Caro, A. Quattrini, L. Valli, A. Sannino, C. Giannini, Sci. Rep. 2018, 8, 1429.
A. Terzi, N. Gallo, S. Bettini, T. Sibillano, D. Altamura, L. Campa, M. L. Natali, L. Salvatore, M. Madaghiele, L. De Caro, L. Valli, A. Sannino, C. Giannini, Front. Bioeng. Biotech. 2019, 7, 203.
H. J. Hoppe, K. B. Reid, Protein Sci. 1994, 3, 1143.
K. Håkansson, K. B. Reid, Protein Sci. 2000, 9, 1607.
T. Koide, K. Nagata, Collagen 2005, 85.
D. J. Prockop, K. I. Kivirikko, L. Tuderman, N. A. Guzman, N. Engl. J. Med. 1979, 301, 13.
P. F. Davison, B.-S. Hong, D. J. Cannon, Exp. Eye Res. 1979, 29, 97.
A. McAlinden, T. A. Smith, L. J. Sandell, D. Ficheux, D. A. D. Parry, D. J. S. Hulmes, J. Biol. Chem. 2003, 278, 42200.
J. Uitto, R. E. Allan, K. L. Polak, Eur. J. Biochem. 1979, 99, 97.
K Nakai, M. Kanehisa, Genomics 1992, 14, 897.
K. Nagata, Matrix Biol. 1998, 16, 379.
L. Bonfanti, A. A. Mironov, Jr., J. A. Martínez-Menárguez, O. Martella, A. Fusella, M. Baldassarre, R. Buccione, H. J. Geuze, A. A. Mironov, A. Luini, Cell 1998, 95, 993.
D. J. Prockop, K. I. Kivirikko, Annu. Rev. Biochem. 1995, 64, 403.
K. M. Meek, G. F. Elliott, Z. Sayers, S. B. Whitburn, M. H. J. Koch, J. Mol. Biol. 1981, 149, 477.
T. J. Wess, Adv. Protein Chem. 2005, 70, 341.
M. Koch, J. Schulze, U. Hansen, T. Ashwodt, D. R. Keene, W. J. Brunken, R. E. Burgeson, P. Bruckner, L. Bruckner-Tuderman, J. Biol. Chem. 2004, 279, 22514.
D. R. Keene, J. Cell Biol. 1987, 105, 2393.
E. Adachi, I. Hopkinson, T. Hayashi, Int. Rev. Cytol. 1997, 173, 73.
A. V. Persikov, R. J. Pillitteri, P. Amin, U Schwarze, P. H. Byers, B. Brodsky, Hum. Mutat. 2004, 24, 330.
G. N. Ramachandran, G. Kartha, Nature 1955, 176, 593.
J. Bella, B. Brodsky, H. B. Berman, Structure 1995, 3, 893.
M.-M. Giraud-Guille, J. Mol. Biol. 1992, 224, 861.
J. E. Scott, Int. J. Biol. Macromol. 1991, 13, 157.
H. S. Gupta, J. Seto, S. Krauss, P. Boesecke, H. R. Screen, J. Struct. Biol. 2010, 169, 183.
B. Brodsky, J. A. Ramshaw, Matrix Biol. 1997, 15, 545.
M. D. Shoulders, R. T. Raines, Annu. Rev. Biochem. 2009, 78, 929.
R. Fleischmajer, E. Douglas MacDonald, J. S. Perlish, R. E. Burgeson, L. W. Fisher, J. Struct. Biol. 1990, 105, 162.
L. I. Smith-Mungo, H. M. Kagan, Matrix Biol. 1998, 16, 387.
R. Parenteau-Bareil, R. Gauvin, F. Berthod, Materials 2010, 3,1863.
L. Cen, W. Liu, L. Cui, W. Zhang, Y. Cao, Pediatr. Res. 2008, 63, 492.
E. J. Miller, in Collagen Vol. I - Biochemistry, (Ed: M. E. Nimni), CRC Press, Boca Raton, FL 1988, pp. 139-157.
M. E. Nimni, D. Cheung, B. Strates, M. Kodama, K. Sheikh, J. Biomed. Mater. Res. 1987, 21, 741.
Z. R. Li, B. Wang, C. F. Chi, Q. H. Zhang, Y. D. Gong, J. J. Tang, H. Y. Luo, G. F. Ding, Food Hydrocolloids 2013, 31, 103.
M. H. Santos, R. M. Silva, V. C Dumont, J. S. Neves, H. S. Mansur, L. G. D. Heneine, Mater. Sci. Eng., C 2013, 33, 790.
N. Muralidharan, R. J. Shakila, D. Sukumar, G. Jeyasekaran, J. Food Sci. Technol. 2013, 50, 1106.
R. L. Trelstad, in Immunochemistry of the Extracellular Matrix, Vol. I Methods (Ed: H. Furthmayer), CRC Press, Boca Raton, FL 1982, pp. 32-39.
G. Cioca, US Patent 4279812, 1981.
M. Roreger, PCT WO 95/28964, 1995.
K. A. Piez, in Encyclopedia of Polymer Science and Engineering (Ed: J. I. Kroschwitz), Wiley, New York 1985, pp. 699-727.
E. J. Miller, in Extracellular Matrix Biochemistry (Eds: K. A. Piez, A. H. Reddi), Elsevier, New York 1984, pp. 41-82.
T. R. Knapp, E. Luck, J. R. Daniels, J. Surg. Res. 1977, 23, 96.
K. A. Piez, in Extracellular Matrix Biochemistry (Eds: K. A. Piez, A. H. Reddi), Elsevier, New York 1984, pp. 1-40.
S. L. Lee, Collagen Relat. Res. 1983, 3, 305.
H. R. C. Screen, D. L. Bader, D. A. Lee, J. C. Shelton, Strain 2004, 40, 157.
M. Franchi, A. Trirè, M. Quaranta, E. Orsini, V. Ottani, Sci. World J. 2007, 7, 404.
F. H. Silver, J. W. Freeman, G. P. Seehra, J. Biomech. 2003, 36, 1529.
J. M. Squire, A. Freundlich, Nature 1980, 288, 410.
V. Ottani, M. Raspanti, A. Ruggeri, Micron 2001, 32, 251.
E. Reale, F. Benazzo, A. Ruggeri, J. Sub. Cytol. 1981, 13, 135.
F. H. Silver, Y. P. Kato, M. Ohno, A. J. Wasserman, J. Long Term Eff. Med. Implants 1992, 2, 165.
T. Y. Kostrominova, S. V. Brooks, Age 2013, 35, 2203.
L. Jozsa, P. Kannus, Anatomy, Physiology and Pathology, Human Kinetics, Champaign, IL 1997.
S. Rosager, P. Aagaard, P. Dyhre-Poulsen, K. Neergaard, M. Kjaer, S. P. Magnusson, Scand. J. Med. Sci. Sports 2002, 12, 90.
S. L. Woo, M. A. Ritter, D. Amiel, T. M. Sanders, M. A. Gomez, S. C. Kuei, S. R. Garfin, W. H. Akeson, Connect. Tissue Res. 1980, 7, 177.
C. I. Buchanan, R. L. Marsh, J. Appl. Physiol. 2001, 90, 164.
M. Marchini, M. Morocutti, A. Ruggeri, M. H. J. Koch, A. Bigi, N. Roveri, Connect. Tissue Res. 1986, 15, 269.
E. Fuchs, Curr. Top. Dev. Biol. 2016, 116, 357.
L. Józsa, P. Kannus, Scand. J. Med. Sci. Sports 1997, 7, 113.
J. D. Eekhoff, F. Fang, S. P. Lake, Connect. Tissue Res. 2018, 59, 410.
F. Fang, S. P. Lake, J. Orthop. Res. 2015, 33, 1704.
F. Bianchi, F. Hofmann, A. J. Smith, M. S. Thompson, Acta Biomater. 2016, 45, 321.
K. Vig, A. Chaudhari, S. Tripathi, S. Dixit, R. Sahu, S. Pillai, V. A. Dennis, S. R. Singh, Int. J. Mol. Sci. 2017, 8, E789.
W. Li, Biomed. Eng. Lett. 2015, 5, 241.
W. D. Losquadro, Facial Plast. Surg. Clin. North Am. 2017, 25, 283.
R. Wong, S. Geyer, W. Weninger, J. C. Guimberteau, J. K. Wong, Exp. Dermatol. 2016, 25, 92.
H. T. Cox, Br. J. Surg. 1941, 29, 234.
M. D. Ridge, V. Wright, J. Invest. Dermatol. 1966, 46, 341.
T. Gibson, R. M. Kenedi, J. E. Craik, Br. J. Surg. 1965, 52, 764.
T. Miyata, T. Taira, Y. Noishiki, Clin. Mater. 1992, 9, 139.
M. Gingras, M. M. Beaulieu, V. Gagnon, H. D. Durham, F. Berthod, Glia 2008, 56, 354.
Z. M. Che, T. H. Jung, J. H. Choi, J. D. Yoon, H. J. Jeong, E. J. Lee, J. Kim, Biochem. Biophys. Res. Commun. 2006, 346, 268.
F. Sabeh, R. Shimizu-Hirota, S. J. Weiss, J. Cell Biol. 2009, 185, 11.
N. Shanmugasundaram, P. Ravichandran, P. N. Reddy, N. Ramamurty, S. Pal, K. P. Rao, Biomaterials 2001, 22, 1943.
C. H. Lee, A. Singla, Y. Lee, Int. J. Pharm. 2001, 221, 1.
H. Sumiyoshi, F. Laub, H. Yoshiok, Dev. Dyn. 2001, 220, 155.
A. Sionkowska, Polym. Int. 2016, 65, 1123.
A. Sionkowska, J. Kozłowska, Int. J. Biol. Macromol. 2013, 52, 250.
X. Wang, L. Sang, D. Luo, X. Li, Colloids Surf., B. 2011, 82, 233.
D. Thacharodi, K. P. Rao, Int. J. Pharm. 1995, 120, 115.
D. Altamura, S. Pastore, M. G. Raucci, D. Siliqi, F. De Pascalis, M. Nacucchi, L. Ambrosio, C. Giannini, ACS Appl. Mater. Interfaces 2016, 8, 8728.
A. C. Abramo, J. C. Viola, Br. J. Plast. Surg. 1992, 45, 117.
S. Mizuno, J. Glowacki, Biomaterials 1996, 17, 1819.
B. A. Harley, A. K. Lynn, Z. Wissner-Gross, W. Bonfield, I. V. Yannas, L. J. Gibson, J. Biomed. Mater. Res., Part A 2010, 92, 1066.
C. Du, F. Z. Cui, W. Zhang, Q. L. Feng, X. D. Zhu, K. de Groot, J. Biomed. Mater. Res. 2000, 50, 518.
I. V. Yannas, J. F. Burke, D. P. Orgill, E. M. Skrabut, Science 1982, 215, 174.
C. Nie, D. Yang, S. F. Morris, Med. Hypotheses 2009, 72, 679.
A. M. Altman, N. Matthias, Y. Yan, Y. H. Song, X. Bai, E. S. Chiu, D. P. Slakey, E. U. Alt, Biomaterials 2008, 29, 1431.
A. Sano, M. Maeda, S. Nagahara, T. Ochiya, K. Honma, H. Itoh, T. Miyata, K. Fujioka, Adv. Drug Delivery Rev. 2003, 55, 1651.
M. Griffith, W. B. Jackson, N. Lagali, K. Merrett, F. Li, P. Fagerholm, Eye 2009, 23, 1985.
P. Carrier, A. Deschambeault, M. Talbot, C. J. Giasson, F. A. Auger, S. L. Guerin, L. Germain, Investig. Opthalmol. Vis. Sci. 2008, 49, 1376.
L. J. Chamberlain, I. V. Yannas, H. P. Hsu, G. Strichartz, M. Spector, Exp. Neurol. 1998, 154, 315.
W. Colin, R. B. Donoff, J. Dent. Res. 1984, 63, 987.
W. Sun, H. Lin, B. Chen, W. Zhao, Y. Zhao, Z. Xiao, J. Dai, J. Biomed. Mater. Res., Part A 2009, 92A, 887.
W. Sun, H. Lin, B. Chen, W. Zhao, Y. Zhao, J. Dai, J. Biomed. Mater. Res., Part A 2007, 83A, 1054.
M. Gingras, I. Paradis, F. Berthod, Biomaterials 2003, 24, 1653.
M. Blais, M. Grenier, F. Berthod, J. Invest. Dermatol. 2009, 129, 2895.
R. H. Keates, E. Martines, D. G. Tennen, C. Reich, J. Cataract Refract. Surg. 1995, 21, 519.
D. R. Jung, R. Kapur, T. Adams, K. A. Giuliano, M. Mrksic, H. G. Craighead, D. L. Taylor, Crit. Rev. Biotechnol. 2001, 21, 111.
M. Mrksich, Cell. Mol. Life Sci. 1998, 54, 653.
C. Y. Tay, S. A. Irvine, F. Y. Boey, L. P. Tan, S. Venkatraman, Small 2011, 7, 1361.
Y. Ito, Biomaterials 1999, 20, 2333.
A. Rich, F. H. C. Crick, J. Mol. Biol. 1961, 3, 483.
K. Okuyama, X. Xu, M. Iguchi, K. Noguchi, Biopolymers 2006, 84, 181.
K. Okuyama, Connect. Tissue Res. 2008, 49, 299.
K. Okuyama, K. Miyama, K. Mizuno, H. P. Bächinger, Biopolymers 2012, 97, 607.
B. L. Trus, K. Piez, Nature 1980, 286, 300.
J. P. R. O. Orgel, T. C. Irving, A. Miller, T. J. Wess, Proc. Natl. Acad. Sci. USA 2006, 103, 9001.
P. Fratzl, K. Misof, I. Zizak, G. Rapp, H. Amenitsch, S. Bernstorff, J. Struct. Biol. 1998, 122, 119.
P. Fratzl, N. Fratzl-Zelman, K. Klaushofer, Biophys. J. 1993, 64, 260.
C. Giannini, D. Siliqi, M. Ladisa, D. Altamura, A. Diaz, A. Beraudi, T. Sibillano, L. De Caro, S. Stea, F. Baruffaldi, O. Bunk, J. Appl. Crystallogr. 2014, 47, 110.
R. Puxkandl, I. Zizak, O. Paris, J. Keckes, W. Tesch, S. Bernstorff, P. Fratzl, Philos. Trans. R. Soc. Lond. B Biol. Sci. 2002, 357, 191.
N. Sasaki, N. Shukunami, N. Matsushima, Y. Izumi, J. Biomech. 1999, 32, 285.
V. J. James, Int. J Cancer 2009, 125, 133.
G Suarez, A. L. Oronsky, J. Bordas, M. H. Koch, Proc. Natl. Acad. Sci. USA 1985, 82, 4693.
D. Altamura, R. Lassandro, F. A. Vittoria, L. De Cari, D. Siliqi, M. Ladisa, C. Giannini, J. Appl. Crystallogr. 2012, 45, 869.
D. Siliqi, L. De Caro, M. Ladisa, F. Scattarella, A. Mazzone, D. Altamura, T. Sibillano, C. Giannini, J. Appl. Crystallogr. 2016, 49, 1107.
L. Sun, H. Hou, B. Li, Y. Zhang, Int. J. Biol. Macromol. 2017, 99, 8.
T. Sibillano, L. De Caro, F. Scattarella, G. Scaracelli, D. Siliqi, D. Altamura, M. Liebi, M. Ladisa, O. Bunk, C. Giannini, J. Appl. Crystallogr. 2016, 49, 1231.
C. Giannini, A. Terzi, L. Fusaro, T. Sibillano, A. Diaz, M. Ramella, V. Lutz-Bueno, F. Boccafoschi, O. Bunk, J. Biophotonics 2019, 12, e201900106.
G. J. Cameron, I. L. Alberts, J. H. Laing, T. J. Wess, J. Struct. Biol. 2002, 137, 15.
A. Barth, Biochim. Biophys. Acta,- Bioenerg. 2007, 1767, 1073.
Y. Huayan, Y. Shouning, K. Jilie, D. Aichun, Y. Shaoning, Nat. Protoc. 2015, 10, 382.
S. D. Figueiró, J. CGóes, R. A. Moreira, A. S. B. Sombra, Carbohydr. Polym. 2004, 56, 313.
V. Renugopalakrishnan, G. Chandrakasan, S. Moore, T. B. Hutson, C. V. Berney, RajendraS. Bhatnagar, Macromolecules 1989, 22, 4121.
C. Petibois, G. Gouspillou, K. Wehbe, J. P. Delage, G. Déléris, Anal. Bioanal. Chem. 2006, 386, 1961.
E. Goormaghtigh, J. M. Ruysschaert, V. Raussens, Biophys. J. 2006, 90, 2946.
R. Puxkandl, I. Zizak, O. Paris, J. Keckes, W. Tesch, S. Bernstorff, P. Purslow, P Fratzl, Philos. Trans. R. Soc. Lond.B, Biol. Sci. 2002, 357, 191.
S. J. Eppell, B. N. Smith, H. Kahn, R. Ballarini, J. R. Soc., Interface 2006, 3, 117.
D. P. Pioletti, L. R. Rakotomanana, Eur. J. Mech- A: Solids 2000, 19, 749.
N. A. Manssor, Z. Radzi, N. A. Yahy, L Mohamad Yusof, F. Hariri, N. H. Khairuddin, N. H. Abu Kasim, J. T. Czernuszka, Skin Pharmacol. Physiol. 2016, 29, 55.
L. H. H. Damink, P. J. Dijkstra, M. J. A. van Luyn, P. B. van Wachem, P. Nieuwenhuis, J. Feijen, J. Mater. Sci.: Mater. Med. 1995, 6, 460.
P. Angele, J. Abke, R. Kujat, H. Faltermeier, D. Schumann, M. Nerlich, B. Kinner, C. Englert, Z. Ruszczak, R. Mehrl, R. Mueller, Biomaterials 2004, 25, 2831.
H. Notbohm, S. Mosler, M. Bodo, C. Yang, H. Lehmann, B. Batge, P. K Muller, J. Protein Chem. 1992, 11, 635.

Auteurs

Alberta Terzi (A)

Institute of Crystallography (IC), National Research Council, Bari, 70126, Italy.

Nunzia Gallo (N)

Department of Engineering for Innovation, University of Salento, Lecce, 73100, Italy.

Simona Bettini (S)

Department of Engineering for Innovation, University of Salento, Lecce, 73100, Italy.

Teresa Sibillano (T)

Institute of Crystallography (IC), National Research Council, Bari, 70126, Italy.

Davide Altamura (D)

Institute of Crystallography (IC), National Research Council, Bari, 70126, Italy.

Marta Madaghiele (M)

Department of Engineering for Innovation, University of Salento, Lecce, 73100, Italy.

Liberato De Caro (L)

Institute of Crystallography (IC), National Research Council, Bari, 70126, Italy.

Ludovico Valli (L)

Department of Biological and Environmental Sciences and Technologies, University of Salento, Lecce, 73100, Italy.

Luca Salvatore (L)

Department of Engineering for Innovation, University of Salento, Lecce, 73100, Italy.

Alessandro Sannino (A)

Department of Engineering for Innovation, University of Salento, Lecce, 73100, Italy.

Cinzia Giannini (C)

Institute of Crystallography (IC), National Research Council, Bari, 70126, Italy.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH